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Plasmodium Knowlesi Siner et al. Malar J (2017) 16:417 DOI 10.1186/s12936-017-2064-9 Malaria Journal RESEARCH Open Access Absence of Plasmodium inui and Plasmodium cynomolgi, but detection of Plasmodium knowlesi and Plasmodium vivax infections in asymptomatic humans in the Betong division of Sarawak, Malaysian Borneo Angela Siner* , Sze‑Tze Liew, Khamisah Abdul Kadir, Dayang Shuaisah Awang Mohamad, Felicia Kavita Thomas, Mohammad Zulkarnaen and Balbir Singh* Abstract Background: Plasmodium knowlesi, a simian malaria parasite, has become the main cause of malaria in Sarawak, Malaysian Borneo. Epidemiological data on malaria for Sarawak has been derived solely from hospitalized patients, and more accurate epidemiological data on malaria is necessary. Therefore, a longitudinal study of communities afected by knowlesi malaria was undertaken. Methods: A total of 3002 blood samples on flter paper were collected from 555 inhabitants of 8 longhouses with recently reported knowlesi malaria cases in the Betong Division of Sarawak, Malaysian Borneo. Each longhouse was visited bimonthly for a total of 10 times during a 21-month study period (Jan 2014–Oct 2015). DNA extracted from blood spots were examined by a nested PCR assay for Plasmodium and positive samples were then examined by nested PCR assays for Plasmodium falciparum, Plasmodium vivax, Plasmodium malariae, Plasmodium ovale, Plasmodium knowlesi, Plasmodium cynomolgi and Plasmodium inui. Blood flms of samples positive by PCR were also examined by microscopy. Results: Genus-specifc PCR assay detected Plasmodium DNA in 9 out of 3002 samples. Species-specifc PCR identi‑ fed 7 P. knowlesi and one P. vivax. Malaria parasites were observed in 5 thick blood flms of the PCR positive samples. No parasites were observed in blood flms from one knowlesi-, one vivax- and the genus-positive samples. Only one of 7 P. knowlesi-infected individual was febrile and had sought medical treatment at Betong Hospital the day after sam‑ pling. The 6 knowlesi-, one vivax- and one Plasmodium-infected individuals were afebrile and did not seek any medical treatment. Conclusions: Asymptomatic human P. knowlesi and P. vivax malaria infections, but not P. cynomolgi and P. inui infec‑ tions, are occurring within communities afected with malaria. Keywords: Plasmodium knowlesi, Malaria, Asymptomatic, Submicroscopic Background Plasmodium vivax, Plasmodium ovale and Plasmodium Prior to 2004, human malarias were thought to be caused malariae. Discovery of a large number of Plasmodium by four species of Plasmodium; Plasmodium falciparum, knowlesi cases in the Kapit division of Sarawak [1] led to the inclusion of P. knowlesi, a simian malaria parasite [2], *Correspondence: [email protected]; [email protected] as the ffth cause of malaria in humans [3]. Morphologi- Malaria Research Centre, Faculty of Medicine and Health Sciences, cal similarities between P. knowlesi and P. malariae, when Universiti Malaysia Sarawak, 94300 Kota Samarahan, Sarawak, Malaysia examined by microscopy, had led to P. knowlesi being © The Author(s) 2017. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Siner et al. Malar J (2017) 16:417 Page 2 of 11 misdiagnosed mainly as P. malariae [4]. Plasmodium PCR resulted in the detection of more P. knowlesi posi- knowlesi infections have been reported in other states in tive samples: 67/372 (18%), 71/335 (21.9%) and 60/289 Malaysia [5–9] and in other Southeast Asian countries, (20.7%), respectively. Only one of the 1147 asymptomatic including Tailand [10, 11], Philippines [12], Singapore individuals was positive by microscopy [29]. [13], Myanmar [14], Indonesia [15], Cambodia [16] and Plasmodium knowlesi is typically found in nature in Vietnam [17]. long-tailed and pig-tailed macaques [23]. Other simian Plasmodium knowlesi is the most common cause of malaria parasites, such as Plasmodium cynomolgi and malaria in Sarawak. Epidemiology data for 2014–2015 Plasmodium inui that infect these macaques, have also showed that P. knowlesi was responsible for 82.9% of the been shown to be capable of inducing malaria in humans 2174 malaria cases diagnosed in Sarawak [18]. Studies through mosquito bites under experimental conditions over the past 10 years in Sarawak by the Malaria Research [23] and there has been one case of a natural infec- Centre, UNIMAS, using nested PCR assays [1, 19], have tion of a woman by P. cynomolgi in Peninsular Malaysia confrmed 890 cases of P. knowlesi and only 6 cases of P. [30]. Both P. cynomolgi and P. inui have been described malariae [20]. Since all 6 patients were Sarawakians who in wild macaques in Sarawak [31]. Since these parasites had been working in logging camps overseas in malaria occur in the same reservoir host as P. knowlesi, there is endemic countries and had recently returned to Sarawak, a strong possibility that natural infections in humans of it indicated that these infections were acquired overseas these simian malaria parasites could occur in Sarawak. and there were no indigenous cases of P. malariae in However, since P. inui is morphologically identical with P. Sarawak. malariae and P. cynomolgi is morphologically similar to Human infections with P. knowlesi cause a wide spec- P. vivax by microscopy [23], these infections have prob- trum of disease, including fatal infections [3, 5, 21]. ably been identifed by routine microscopy as P. malar- Knowlesi malaria induced by mosquito bites under iae or P. vivax. Furthermore, human infections with P. laboratory conditions with the same P. knowlesi strain inui and P. cynomolgi largely resulted in mild infections, produced varying outcomes in humans that included which would not normally require hospitalization [23]. refractory individuals, those that self cured, and others Te recent development of molecular detection methods that required anti-malarial treatment as their infections for simian malaria parasites [31], afords the possibility of were deemed severe [22, 23]. Asymptomatic malaria examining human samples for simian malaria parasites infections have been described for P. falciparum and other than P. knowlesi. Studies utilizing these molecular P. vivax. Although all Plasmodium species can cause detection assays on communities living close to the forest asymptomatic malaria, there have not been many reports fringe, such as those in Betong, would indicate whether of asymptomatic P. malariae [24] and P. ovale [25] infec- other simian malaria parasites are being transmitted to tions. Plasmodium malariae infection may be asympto- humans. Questions relating to whether there are asymp- matic or cause only mild symptoms for many years after tomatic infections, whether there is clustering of cases the initial infection [24]. Detection of these asymptomatic within longhouse communities and whether there is carriers by highly sensitive molecular detection assays human-to-human transmission can be answered by con- has provided a greater understanding of the epidemiol- ducting longitudinal studies in these communities utiliz- ogy of malaria [26, 27]. Studies on P. knowlesi in Sarawak ing molecular detection tools. have been solely hospital-based investigations [1, 5, 8, In this longitudinal study, dried blood spots from 9, 21], but there have been reports of asymptomatic P. individuals living within communities with reported knowlesi infections in Vietnam [28] and more recently malaria cases were repeatedly sampled for the presence in Sabah, Malaysian Borneo [29]. In the Vietnam study, of malaria parasites. Tese longhouse communities were species-specifc SSU rRNA nested PCR screen of 95 in the Betong Division, one of the 12 administrative divi- randomly selected P. malariae samples by PCR revealed sions in Sarawak, in which 161 knowlesi malaria cases 5 to be mixed infections with P. knowlesi. All of them, had been reported in the 3 years preceding the initiation including their family members, were asymptomatic at of this study [18]. sampling time [28]. In the Sabah study, 1147 samples were collected from randomly selected villagers resid- Methods ing at same village as the microscopy-positive patients Study population and blood sample collection as well as members of the patients’ and the selected vil- Participants were recruited from 8 longhouses with resi- lager’s households. P. knowlesi was detected in 20/1147 dents having a history of recent admission with knowlesi (1.7%) samples screened by SSU rRNA nested PCR malaria at Betong hospital (Fig. 1). A review of malaria assays. Te use of cytochrome b nested PCR, SSU rRNA cases in the Betong Division, between 2011 and 2013, real time PCR and chromosome 3 plasmepsin real time identifed the following longhouses with a total of 33 Siner et al. Malar J (2017) 16:417 Page 3 of 11 Fig. 1 Global Positioning System (GPS) coordinates and study identifcation (ID) of the 8 longhouses selected in this study: Nanga Mutok (A, 1˚36′18.1″N, 111˚40′24.7″E, Penebak Ulu (B, 1˚39′9.2″N, 111˚44′15.3″E), Raba Tiput (C, 1˚35′8.2″N, 111˚42′7.5″E), Batu Lintang (D, 1˚30′24.3″N, 111˚36′11.0″E), Begumbang (E, 1˚34′25.4″N, 111˚38′3.4″E), Penyelanih Kiba (F, 1˚33′7.21″N, 111˚37′19.07″E), Nanga Ban (G, 1˚23′46.9″N, 111˚31′4.1″E) and Nanga Keron (H, 1˚27′11.8″N, 111˚37′54.6″E) knowlesi malaria cases: Nanga Mutok (10 cases), Penebak monkeys while farming, hunting or fshing. Tey were Ulu (2 cases), Raba Tiput (6 cases), Batu Lintang (1 case), also asked whether they felt unwell or feverish on the day Penyelanih Kiba (2 cases), Begumbang (3 cases), Nanga of the blood collection.
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